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Журнал микробиологии, эпидемиологии и иммунобиологии. 2016; : 74-85

ПЛАЗМИД-АССОЦИИРОВАННАЯ ВИРУЛЕНТНОСТЬ YERSINIA PSEUDOTUBERCULOSIS И ИНФЕКЦИОННЫЙ ПРОЦЕСС

Сомова Л. М., Шубин Ф. Н., Дробот Е. И., Плехова Н. Г., Ляпун И. Н.

https://doi.org/10.36233/0372-9311-2016-6-74-85

Аннотация

Обобщены данные литературы, касающиеся генетически детерминированных факторов патогенности Y. pseudotuberculosis и ассоциированных с ними проявлений этой инфекции. вызываемой разными плазмидными типами возбудителя. Основное внимание обращено на особенности клеточно-тканевых изменений, опосредованных плазмидой вирулентности pYV, а также эффекты патогенности мало изученной плазмиды pVM82, имеющейся только в штаммах Y. pseudotuberculosis, вызывающих клинико-эпидемическое проявление инфекции в виде дальневосточной скарлатиноподобной лихорадки (ДСЛ). Полученные данные о способности дальневосточных штаммов продуцировать суперантиген YPMa, Y. pseudotuberculosis-производный митоген А, вероятно, свидетельствуют о том, что он играет ключевую роль в патогенезе ДСЛ. Вариабельность повреждений клеток врожденного иммунитета и органов-мишеней, вызываемых различными по вирулентности плазмидными типами Y. pseudotuberculosis, может обусловливать полиморфизм клинико-морфологических проявлений этой инфекции. Углубленное понимание зависимости механизмов иммунопатогенеза болезни от молекулярной характеристики возбудителя раскрывает перспективы усовершенствования диагностики и прогнозирования тяжести течения псевдотуберкулеза и в целом иерсиниозов у человека.
Список литературы

1. ГинцбургАЛ., Шубин Ф.Н., Шовадаева Г.А. Новый признак патогенности, кодируемый плазмидой pVM82 Yersinia pseudotuberculosis. Генетика. 1988, 24 (9): 1562-1571.

2. Долматова Л.С., Заика О.А., Недашковская Е.П., Тимченко Н.Ф. Исследование механизмов апоптоз-модулирующего влияния термостабильного токсина Yersinia pseudotuberculosis и корригирующего действия экстракта из дальневосточных видов голотурий на нейтрофилы крыс in vitro. Тихоокеанский медицинский журнал. 2010, 3: 76-80.

3. Дробот Е.И. Реактивность клеток врожденного иммунитета при инфекции, вызванной разными плазмидными вариантами Y. pseudotuberculosis: Автореф. дис. канд. биол. наук. Владивосток, 2015.

4. Исачкова Л.М., Жаворонков А.А., Антоненко Ф.Ф. Патология псевдотуберкулеза. Владивосток, Дальнаука, 1994.

5. Коновалова Ж. А. Бактерицидные механизмы фагоцитоза Y pseudotuberculosis с разным набором плазмид: Автореф. дис. канд. биол. наук. Иркутск, 2002.

6. ЛитвиноваЛ.В., Ценева Г.Я., Ивашиненко А.П. и др. Генетические особенности Yersinia pseudotuberculosis и эпидемиологические черты групповых заболеваний псевдотуберкулезом в организованных коллективах. Эпидемиология и инфекционные болезни. 2009, 3:31-34.

7. Плехова Н.Г., Дробот Е.И., Тимченко Н.Ф. и др. Влияние термолабильного токсина Yersinia pseudotuberculosis на функции клеток врожденного иммунитета. Бюллетень экспериментальной биологии и медицины. 2014, 157 (4): 483-487.

8. Сомов Г.П. Дальневосточная скарлатиноподобная лихорадка. М., Медицина, 1979.

9. Сомов Г.П., Покровский В.И., Беседнова Н.Н., Антоненко Ф.Ф. Псевдотуберкулез. М., Медицина, 2001.

10. Сомова Л.М., Плехова Н.Г., Дробот Е.И. Новые аспекты патологии псевдотуберкулеза. Архив патологии. 2012, 74 (3): 60-64.

11. Сомова Л.М., Плехова Н.Г., Дробот Е.И. и др. Патоморфологические изменения при экспериментальной токсинемии, вызванной термолабильным токсином Yersinia pseudo-tuberculosis. Тихоокеанский медицинский журнал. 2010, 3: 65-67.

12. Тимченко Н.Ф., Недашковская Е.П., Долматова Л.С., Сомова-Исачкова Л. М. Токсины Yersinia pseudotuberculosis. Владивосток, Приморский полиграфкомбинат, 2004.

13. Ценева Г.Я., Солодовникова Н.Ю., Воскресенская Е.А. Молекулярные аспекты вирулентности иерсиний. Клиническая микробиология и антимикробная химиотерапия. 2002, 3: 248-266.

14. Шубин Ф.Н., Гинцбург А.Л., Китаев В.М. и др. Анализ плазмидного состава штаммов Yersinia pseudotuberculosis и его применение для типирования возбудителя псевдотуберкулеза. Молекулярная генетика, микробиология, вирусология. 1989, 6: 20-25.

15. Шубин Ф.Н., Сибирцев Ю.Т., Рассказов В. А. Плазмиды Yersinia pseudotuberculosis и их значение в реализации эпидемического процесса при псевдотуберкулезе. Журн. микро-биол. 1985, 12: 53-56.

16. Шурыгина И.А., Чеснокова М.В., Климов В.Т. и др. Псевдотуберкулез. Новосибирск, Наука, 2003.

17. Achtman М., Zurth К., Morelli С. et al. Yersinia pestis, a cause of plaque, is a recently emerged clone of Yerswinia pseudotuberculosis. Proc. Natl. Acad. Sci. USA. 1999, 96: 14043-14048.

18. Bergsbaken T, Cookson B.T. Macrophage activation redirects Yersinia-infected host cell death from apoptosis to caspase-1-dependent pyroptosis. PLoS Pathog. 2007, 33: el61.

19. Bergsbaken T, Cookson В. T. Innate immune response during Yersinia infection: critical modulation of cell death mechanisms through phagocyte activation. J. Leukoc. Biol. 2009, 86 (5): 1153-1158.

20. Blank C., Luz A., Bending S. et al. Superantigen and endotoxin synergize in the induction of lethal shock. Eur. J. Immunol. 1997, 27: 825-833.

21. Brodsky I.E., R. Medzhitov R. Reduced secretion of YopJ by Yersinia limits in vivo cell death but enhances bacterial virulence. PLoS Pathog. 2008. 4: el000067.

22. Brodsky I.E., Palm N.W., Sadanand S. et al. Yersinia effector protein promotes virulence by preventing inflammasome recognition of the type III secretion system. Cell. Host. Microbe. 2010, 7 (5): 376-387.

23. Comelis G. The type III secretion injectisome, a complex nanomachine for intracellular ‘toxin’ delivery. Biol. Chem. 2010, 391 (7): 745-751.

24. Dube P. Interaction of Yersinia with the gut: mechanisms of pathogenesis and immune evasion. Curr. Top. Microbiol. Immunol. 2009, 337: 61-91.

25. Eppinger M., Rosovitz M.J., Fricke W.F. et al. The complete genome sequence of Yersinia pseudotuberculosis IP31758, the causative agent of Far Easr scarlet-like fever. PLos Genet. 2007, 3: el42.

26. Femandes-Alnemri T, Wu J., Yu J.W. et al. The pyroptosome: a supramolecular assembly of ASC dimers mediating inflammatory cell death via caspase-1 activation. Cell Death Differ. 2007, 14: 1590-1604.

27. Fink S.L., Cookson B.T. Apoptosis, pyroptosis, and necrosis: mechanistic description of dead and dying eukaryotic cells. Infect. Immun. 2005, 73: 1907-1916.

28. FukushimaH., MatsudaY., Seki R. Geographical heterogenicity between Far East and Wfestem countries in prevalence of the virulence plasmid, the superantigen Yersinia pseudotuberculosis derived mitogen and the high-pathogenicity island among Yersinia pseudotuberculosis strains. J. Clin. Microbiol. 2001, 39: 3541-3547.

29. Jardetzky T.S., Brown J.H., Gorda J.C. et al. Three-dimensional structure of human class II histocompatibility molecule complexed with superantigen. Nature. 1994, 368: 711-718.

30. Labbe K., Mclntire C.R., Doiron K. et al. Cellular inhibitors of apoptosis proteins cIAP2 are required for efficient caspase-1 activation by the inflammasome. Immunity. 2011, 35 (6): 897-907.

31. Lilo S., Zheng Y., Bliska J.B. Caspase-1 activation in macrophages infected with Yersinia pestis KIM requires the type III secretion system effector YopJ. Infect. Immun. 2008, 76: 3911-3923.

32. Marketon M.M., DePaolo R.W., DeBord R.W. et al. Plaque bacteria target immune cells during infection. Science. 2005, 309: 1739-1741.

33. Medzhitov R., Schneider D.S., Soares M.P. Disease tolerance as a defense strategy. Science. 2012, 335 (6071): 936-941.

34. Meinzer U., Barreau E, Esmiol-Welterlin S. et al. Yersinia pseudotuberculosis effector YopJ subverts the Nod2 rick Takl pathway and activates caspase-1 to induce intestinal barrier dysfunction. Ceil. Host. Microbe. 2012,11 (4): 337-351.

35. Miyoshi-AkiyamaT., FujimakiW., YanX.J. et al. Identification of murine T cells reactive with the bacterial superantigen Y. pseudotuberculosis - derived mitogen (YPM) and factors involved in YPM-induced toxicity in mice. Microbiol. Immunol. 1997, 41: 345-352.

36. Moreau K., Lacas-Gervis S., Fujita N. et al. Autophagosomes can support Yersinia pseudotuberculosis replication in macrophages. Cell. Microbiol. 2010, 12 (8): 108-123.

37. Norenberg D., Wieser A., Magistro G. et al. Molecular analysis of a novel Toll/interleukin-1 receptor (TIR)-doman containing virulence protein of Y. pseudotuberculosis among Far East scarlet-like fever serotype I strains. Intern. J. Med. Microbiol. 2013, 303: 583-594.

38. Loughlin J.L., Spinner J.L., Minnich S.A., Kobayashi S.D. Yersinia pestis two-component gene regulatory systems promote survival in human neutrophils. Infect. Immun. 2010, 78 (2): 773-782.

39. Peters K.N., Dhariwala M.O., Hughes-Hanks J.M. Early apoptosis of macrophages modulated by injection of Yersinia pestis YopK promotes progression of primary pneumonic plague. PLoS Pathog. 2013, 9 (4): el003324.

40. Sanmun D., Witasp E., Jitkaew S. et al. Involvment of a functional NADPH oxidase in neutrophils and macrophages during programmed cell clearance: implications for chronic granulomatous disease. Am. J. Physiol. Cell Physiol. 2009, 3: 621-631.

41. Sato K., Ouchi K., Taki M. et al. Yersinia pseudotuberculosis infection in children, resembling Izumi fever and Kawasaki syndrome. Pediatr. Infect. Dis. 1983, 2: 123-126.

42. Savina C., Martina L., Bouchierb Ch. et al. The Yersinia pseudotuberculosis complex: Characterization and delineation of a new species, Yersinia wautersii. Intern. J. Med. Microbiol. 2014, 304: 452-463.

43. Shao F. Biochemical functions of Yersinia type III effectors. Curr. Opin. Microbiol. 2008, 11: 21-29.

44. Silva M.T. When two is better than one: macrophages and neutrophils work in concert in innate immunity as complementary and cooperative partners of a myeloid phagocyte system. J. Leukoc. Biol. 2010, 87(1): 93-106.

45. Spinner J.L., CundiffJ.A., Kobayashi S.D. Yersinia pestis type III secretion system-dependent inhibition of human polymorphonuclear leukocyte function. Infect. Immun. 2008, 76: 3754-3760.

46. Spinner J.L., Seo K.S., O’Loughlin J.L. et al. Neutrophils are resistant to Yersinia YopJ/P-induced apoptosis and are protected from ROS-mediated cell death by the type III secretion system. PLoS One. 2010, 18: e9279.

47. TsenevaG.Y., ChesnokovaM.V., Klimov V.T. etal. Pseudotuberculosis in the Russian Federation. Adv. Exp. Med. Biol. 2012, 954: 63-68.

48. Tsubokura M., Orsuki K., Sato K. et al. Special features of distribution of Yersinia pseudotuberculosis in Japan. J. Clin. Microbiol. 1989, 27: 790-791.

49. Zauberman A., Cohen S., Mamroud E. et al. Interaction of Yersinia pestis with macrophages: limitations in YopJ-dependent apoptosis. Infect. Immun. 2006, 74: 3239-3250.

50. ZippeliusA., Pittet M.J., Batard P. et al. Thymus selection generates a large T cell pool recognizing a self-peptide in humans. J. Exp. Med. 2002, 195: 485-494.

51. Zhang Y., Murtha J., Roberts M.A. et al. Type III secretion decreases bacterial and host survival following phagocytosis of Yersinia pseudotuberculosis by macrophages. Infect. Immun. 2008, 76 (9): 4299-4310.

52. Zheng Y., Lilo S., Mena R, Bliska J.B. YopJ-induced caspase-1 activation in Yersinia-infected macrophages: independent of apoptosis, linked to necrosis, dispensable for innate host defense. PloS One. 2012, 7: e36019.

53. Viboud G.I., Bliska J.B. Yersinia outer proteins: role in modulation of host cell signaling responses and pathogenesis. Annu. Rev. Microbiol. 2005, 59: 69-89.

Journal of microbiology, epidemiology and immunobiology. 2016; : 74-85

PLASMID-ASSOCIATED VIRULENCE OF YERSINIA PSEUDOTUBERCULOSIS AND INFECTIOUS PROCESS

Somova L. M., Shubin F. N., Drobot E. I., Plekhova N. G., Lyapun I. N.

https://doi.org/10.36233/0372-9311-2016-6-74-85

Abstract

Literature data regarding genetically determined pathogenicity factors of Y. pseudotuberculosis and associated manifestations of this infection caused by various plasmid types of the causative agent are generalized. Principal attention is given to features of cell-tissue alterations mediated by virulence plasmid pYV, as well as effects of pathogenicity of an understudied pVM82 plasmid present only in Y. pseudotuberculosis strains causing clinical-epidemic manifestation of the infections as Far East scarlet-like fever (FESLF). The data obtained on the abihty of far-eastern strains to produce YPMa super-antigen, Y. pseudotuberculosis-derivative mitogen A, probably give evidence on its key role in FESLF pathogenesis. Variability of damage of innate immunity cells and target-organs caused by various plasmid types of Y. pseudotuberculosis by virulence could determine polymorphism of clinical-morphological manifestations of this infection. In-depth understanding of dependency of immune pathogenesis mechanisms of the disease on molecular characteristics of the causative agent opens up perspectives of enhancement of diagnostics and prognosis of the severity of the course of pseudotuberculosis and yersiniosis in human in general.
References

1. GintsburgAL., Shubin F.N., Shovadaeva G.A. Novyi priznak patogennosti, kodiruemyi plazmidoi pVM82 Yersinia pseudotuberculosis. Genetika. 1988, 24 (9): 1562-1571.

2. Dolmatova L.S., Zaika O.A., Nedashkovskaya E.P., Timchenko N.F. Issledovanie mekhanizmov apoptoz-moduliruyushchego vliyaniya termostabil'nogo toksina Yersinia pseudotuberculosis i korrigiruyushchego deistviya ekstrakta iz dal'nevostochnykh vidov goloturii na neitrofily krys in vitro. Tikhookeanskii meditsinskii zhurnal. 2010, 3: 76-80.

3. Drobot E.I. Reaktivnost' kletok vrozhdennogo immuniteta pri infektsii, vyzvannoi raznymi plazmidnymi variantami Y. pseudotuberculosis: Avtoref. dis. kand. biol. nauk. Vladivostok, 2015.

4. Isachkova L.M., Zhavoronkov A.A., Antonenko F.F. Patologiya psevdotuberkuleza. Vladivostok, Dal'nauka, 1994.

5. Konovalova Zh. A. Bakteritsidnye mekhanizmy fagotsitoza Y pseudotuberculosis s raznym naborom plazmid: Avtoref. dis. kand. biol. nauk. Irkutsk, 2002.

6. LitvinovaL.V., Tseneva G.Ya., Ivashinenko A.P. i dr. Geneticheskie osobennosti Yersinia pseudotuberculosis i epidemiologicheskie cherty gruppovykh zabolevanii psevdotuberkulezom v organizovannykh kollektivakh. Epidemiologiya i infektsionnye bolezni. 2009, 3:31-34.

7. Plekhova N.G., Drobot E.I., Timchenko N.F. i dr. Vliyanie termolabil'nogo toksina Yersinia pseudotuberculosis na funktsii kletok vrozhdennogo immuniteta. Byulleten' eksperimental'noi biologii i meditsiny. 2014, 157 (4): 483-487.

8. Somov G.P. Dal'nevostochnaya skarlatinopodobnaya likhoradka. M., Meditsina, 1979.

9. Somov G.P., Pokrovskii V.I., Besednova N.N., Antonenko F.F. Psevdotuberkulez. M., Meditsina, 2001.

10. Somova L.M., Plekhova N.G., Drobot E.I. Novye aspekty patologii psevdotuberkuleza. Arkhiv patologii. 2012, 74 (3): 60-64.

11. Somova L.M., Plekhova N.G., Drobot E.I. i dr. Patomorfologicheskie izmeneniya pri eksperimental'noi toksinemii, vyzvannoi termolabil'nym toksinom Yersinia pseudo-tuberculosis. Tikhookeanskii meditsinskii zhurnal. 2010, 3: 65-67.

12. Timchenko N.F., Nedashkovskaya E.P., Dolmatova L.S., Somova-Isachkova L. M. Toksiny Yersinia pseudotuberculosis. Vladivostok, Primorskii poligrafkombinat, 2004.

13. Tseneva G.Ya., Solodovnikova N.Yu., Voskresenskaya E.A. Molekulyarnye aspekty virulentnosti iersinii. Klinicheskaya mikrobiologiya i antimikrobnaya khimioterapiya. 2002, 3: 248-266.

14. Shubin F.N., Gintsburg A.L., Kitaev V.M. i dr. Analiz plazmidnogo sostava shtammov Yersinia pseudotuberculosis i ego primenenie dlya tipirovaniya vozbuditelya psevdotuberkuleza. Molekulyarnaya genetika, mikrobiologiya, virusologiya. 1989, 6: 20-25.

15. Shubin F.N., Sibirtsev Yu.T., Rasskazov V. A. Plazmidy Yersinia pseudotuberculosis i ikh znachenie v realizatsii epidemicheskogo protsessa pri psevdotuberkuleze. Zhurn. mikro-biol. 1985, 12: 53-56.

16. Shurygina I.A., Chesnokova M.V., Klimov V.T. i dr. Psevdotuberkulez. Novosibirsk, Nauka, 2003.

17. Achtman M., Zurth K., Morelli S. et al. Yersinia pestis, a cause of plaque, is a recently emerged clone of Yerswinia pseudotuberculosis. Proc. Natl. Acad. Sci. USA. 1999, 96: 14043-14048.

18. Bergsbaken T, Cookson B.T. Macrophage activation redirects Yersinia-infected host cell death from apoptosis to caspase-1-dependent pyroptosis. PLoS Pathog. 2007, 33: el61.

19. Bergsbaken T, Cookson V. T. Innate immune response during Yersinia infection: critical modulation of cell death mechanisms through phagocyte activation. J. Leukoc. Biol. 2009, 86 (5): 1153-1158.

20. Blank C., Luz A., Bending S. et al. Superantigen and endotoxin synergize in the induction of lethal shock. Eur. J. Immunol. 1997, 27: 825-833.

21. Brodsky I.E., R. Medzhitov R. Reduced secretion of YopJ by Yersinia limits in vivo cell death but enhances bacterial virulence. PLoS Pathog. 2008. 4: el000067.

22. Brodsky I.E., Palm N.W., Sadanand S. et al. Yersinia effector protein promotes virulence by preventing inflammasome recognition of the type III secretion system. Cell. Host. Microbe. 2010, 7 (5): 376-387.

23. Comelis G. The type III secretion injectisome, a complex nanomachine for intracellular ‘toxin’ delivery. Biol. Chem. 2010, 391 (7): 745-751.

24. Dube P. Interaction of Yersinia with the gut: mechanisms of pathogenesis and immune evasion. Curr. Top. Microbiol. Immunol. 2009, 337: 61-91.

25. Eppinger M., Rosovitz M.J., Fricke W.F. et al. The complete genome sequence of Yersinia pseudotuberculosis IP31758, the causative agent of Far Easr scarlet-like fever. PLos Genet. 2007, 3: el42.

26. Femandes-Alnemri T, Wu J., Yu J.W. et al. The pyroptosome: a supramolecular assembly of ASC dimers mediating inflammatory cell death via caspase-1 activation. Cell Death Differ. 2007, 14: 1590-1604.

27. Fink S.L., Cookson B.T. Apoptosis, pyroptosis, and necrosis: mechanistic description of dead and dying eukaryotic cells. Infect. Immun. 2005, 73: 1907-1916.

28. FukushimaH., MatsudaY., Seki R. Geographical heterogenicity between Far East and Wfestem countries in prevalence of the virulence plasmid, the superantigen Yersinia pseudotuberculosis derived mitogen and the high-pathogenicity island among Yersinia pseudotuberculosis strains. J. Clin. Microbiol. 2001, 39: 3541-3547.

29. Jardetzky T.S., Brown J.H., Gorda J.C. et al. Three-dimensional structure of human class II histocompatibility molecule complexed with superantigen. Nature. 1994, 368: 711-718.

30. Labbe K., Mclntire C.R., Doiron K. et al. Cellular inhibitors of apoptosis proteins cIAP2 are required for efficient caspase-1 activation by the inflammasome. Immunity. 2011, 35 (6): 897-907.

31. Lilo S., Zheng Y., Bliska J.B. Caspase-1 activation in macrophages infected with Yersinia pestis KIM requires the type III secretion system effector YopJ. Infect. Immun. 2008, 76: 3911-3923.

32. Marketon M.M., DePaolo R.W., DeBord R.W. et al. Plaque bacteria target immune cells during infection. Science. 2005, 309: 1739-1741.

33. Medzhitov R., Schneider D.S., Soares M.P. Disease tolerance as a defense strategy. Science. 2012, 335 (6071): 936-941.

34. Meinzer U., Barreau E, Esmiol-Welterlin S. et al. Yersinia pseudotuberculosis effector YopJ subverts the Nod2 rick Takl pathway and activates caspase-1 to induce intestinal barrier dysfunction. Ceil. Host. Microbe. 2012,11 (4): 337-351.

35. Miyoshi-AkiyamaT., FujimakiW., YanX.J. et al. Identification of murine T cells reactive with the bacterial superantigen Y. pseudotuberculosis - derived mitogen (YPM) and factors involved in YPM-induced toxicity in mice. Microbiol. Immunol. 1997, 41: 345-352.

36. Moreau K., Lacas-Gervis S., Fujita N. et al. Autophagosomes can support Yersinia pseudotuberculosis replication in macrophages. Cell. Microbiol. 2010, 12 (8): 108-123.

37. Norenberg D., Wieser A., Magistro G. et al. Molecular analysis of a novel Toll/interleukin-1 receptor (TIR)-doman containing virulence protein of Y. pseudotuberculosis among Far East scarlet-like fever serotype I strains. Intern. J. Med. Microbiol. 2013, 303: 583-594.

38. Loughlin J.L., Spinner J.L., Minnich S.A., Kobayashi S.D. Yersinia pestis two-component gene regulatory systems promote survival in human neutrophils. Infect. Immun. 2010, 78 (2): 773-782.

39. Peters K.N., Dhariwala M.O., Hughes-Hanks J.M. Early apoptosis of macrophages modulated by injection of Yersinia pestis YopK promotes progression of primary pneumonic plague. PLoS Pathog. 2013, 9 (4): el003324.

40. Sanmun D., Witasp E., Jitkaew S. et al. Involvment of a functional NADPH oxidase in neutrophils and macrophages during programmed cell clearance: implications for chronic granulomatous disease. Am. J. Physiol. Cell Physiol. 2009, 3: 621-631.

41. Sato K., Ouchi K., Taki M. et al. Yersinia pseudotuberculosis infection in children, resembling Izumi fever and Kawasaki syndrome. Pediatr. Infect. Dis. 1983, 2: 123-126.

42. Savina C., Martina L., Bouchierb Ch. et al. The Yersinia pseudotuberculosis complex: Characterization and delineation of a new species, Yersinia wautersii. Intern. J. Med. Microbiol. 2014, 304: 452-463.

43. Shao F. Biochemical functions of Yersinia type III effectors. Curr. Opin. Microbiol. 2008, 11: 21-29.

44. Silva M.T. When two is better than one: macrophages and neutrophils work in concert in innate immunity as complementary and cooperative partners of a myeloid phagocyte system. J. Leukoc. Biol. 2010, 87(1): 93-106.

45. Spinner J.L., CundiffJ.A., Kobayashi S.D. Yersinia pestis type III secretion system-dependent inhibition of human polymorphonuclear leukocyte function. Infect. Immun. 2008, 76: 3754-3760.

46. Spinner J.L., Seo K.S., O’Loughlin J.L. et al. Neutrophils are resistant to Yersinia YopJ/P-induced apoptosis and are protected from ROS-mediated cell death by the type III secretion system. PLoS One. 2010, 18: e9279.

47. TsenevaG.Y., ChesnokovaM.V., Klimov V.T. etal. Pseudotuberculosis in the Russian Federation. Adv. Exp. Med. Biol. 2012, 954: 63-68.

48. Tsubokura M., Orsuki K., Sato K. et al. Special features of distribution of Yersinia pseudotuberculosis in Japan. J. Clin. Microbiol. 1989, 27: 790-791.

49. Zauberman A., Cohen S., Mamroud E. et al. Interaction of Yersinia pestis with macrophages: limitations in YopJ-dependent apoptosis. Infect. Immun. 2006, 74: 3239-3250.

50. ZippeliusA., Pittet M.J., Batard P. et al. Thymus selection generates a large T cell pool recognizing a self-peptide in humans. J. Exp. Med. 2002, 195: 485-494.

51. Zhang Y., Murtha J., Roberts M.A. et al. Type III secretion decreases bacterial and host survival following phagocytosis of Yersinia pseudotuberculosis by macrophages. Infect. Immun. 2008, 76 (9): 4299-4310.

52. Zheng Y., Lilo S., Mena R, Bliska J.B. YopJ-induced caspase-1 activation in Yersinia-infected macrophages: independent of apoptosis, linked to necrosis, dispensable for innate host defense. PloS One. 2012, 7: e36019.

53. Viboud G.I., Bliska J.B. Yersinia outer proteins: role in modulation of host cell signaling responses and pathogenesis. Annu. Rev. Microbiol. 2005, 59: 69-89.